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C-Myb+ Erythro-Myeloid Progenitor-Derived Fetal Monocytes Give Rise to Adult Tissue-Resident Macrophages
Open accessAbstract
Although classified as hematopoietic cells, tissue-resident macrophages (MFs) arise from embryonic precursors that seed the tissues prior to birth to generate a self-renewing population, which is maintained independently of adult hematopoiesis. Here we reveal the identity of these embryonic precursors using an in utero MF-depletion strategy and fate-mapping of yolk sac (YS) and fetal liver (FL) hematopoiesis. We show that YS MFs are the main precursors of microglia, while most other MFs derive from fetal monocytes (MOs). Both YS MFs and fetal MOs arise from erythro-myeloid progenitors (EMPs) generated in the YS. In the YS, EMPs gave rise to MFs without monocytic intermediates, while EMP seeding the FL upon the establishment of blood circulation acquired c-Myb expression and gave rise to fetal MOs that then seeded embryonic tissues and differentiated into MFs. Thus, adult tissue-resident MFs established from hematopoietic stem cell-independent embryonic precursors arise from two distinct developmental programs.
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“The transcription factors Spi1 and Irf8 have been shown to be the core orchestrators for microglia development”
From Cross-Species Single-Cell Analysis Reveals Divergence of the Primate Microglia Program (2019) · cites this paper as Hoeffel et al., 2015
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“consistent with microglia emerging from PU.1 and IRF8-dependent, but MYB-independent cells 34–37.”
From Efficient derivation of microglia-like cells from human pluripotent stem cells (2016) · cites this paper as [36]
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Fate Mapping Analysis Reveals That Adult Microglia Derive from Primitive Macrophages
Ginhoux, F., Greter, M., Leboeuf, M., Nandi, S., See, P., Gokhan, S., Mehler, M. F., Conway, S. J., Ng, L. G., Stanley, E. R., et al. (2010) · Science · doi:10.1126/science.1194637 · Cited by 5,175
Self-citationBlood Monocytes Consist of Two Principal Subsets with Distinct Migratory Properties
Geissmann, F., Jung, S., & Littman, D. R. (2003) · Immunity · doi:10.1016/s1074-7613(03)00174-2 · Cited by 3,504
Fate Mapping Reveals Origins and Dynamics of Monocytes and Tissue Macrophages under Homeostasis
Yona, S., Kim, K.-W., Wolf, Y., Mildner, A., Varol, D., Breker, M., Strauss-Ayali, D., Viukov, S., Guilliams, M., Misharin, A., et al. (2013) · Immunity · doi:10.1016/j.immuni.2012.12.001 · Cited by 3,245
CCL2 recruits inflammatory monocytes to facilitate breast-tumour metastasis
Qian, B.-Z., Li, J., Zhang, H., Kitamura, T., Zhang, J., Campion, L. R., Kaiser, E. A., Snyder, L. A., & Pollard, J. W. (2011) · Nature · doi:10.1038/nature10138 · Cited by 2,874
A Lineage of Myeloid Cells Independent of Myb and Hematopoietic Stem Cells
Schulz, C., Perdiguero, E. G., Chorro, L., Szabo-Rogers, H., Cagnard, N., Kierdorf, K., Prinz, M., Wu, B., Jacobsen, S. E. W., Pollard, J. W., et al. (2012) · Science · doi:10.1126/science.1219179 · Cited by 2,578
Hematopoiesis: An Evolving Paradigm for Stem Cell Biology
Orkin, S. H., & Zon, L. I. (2008) · Cell · doi:10.1016/j.cell.2008.01.025 · Cited by 2,570
Tissue-resident macrophages originate from yolk-sac-derived erythro-myeloid progenitors
Gomez Perdiguero, E., Klapproth, K., Schulz, C., Busch, K., Azzoni, E., Crozet, L., Garner, H., Trouillet, C., de Bruijn, M. F., Geissmann, F., et al. (2015) · Nature · doi:10.1038/nature13989 · Cited by 2,339
Hashimoto, D., Chow, A., Noizat, C., Teo, P., Beasley, M. B., Leboeuf, M., Becker, C. D., See, P., Price, J., Lucas, D., et al. (2013) · Immunity · doi:10.1016/j.immuni.2013.04.004 · Cited by 2,311
Self-citationVisualizing Spatiotemporal Dynamics of Multicellular Cell-Cycle Progression
Sakaue-Sawano, A., Kurokawa, H., Morimura, T., Hanyu, A., Hama, H., Osawa, H., Kashiwagi, S., Fukami, K., Miyata, T., Miyoshi, H., et al. (2008) · Cell · doi:10.1016/j.cell.2007.12.033 · Cited by 2,194
Pericytes are required for blood–brain barrier integrity during embryogenesis
Daneman, R., Zhou, L., Kebede, A. A., & Barres, B. A. (2010) · Nature · doi:10.1038/nature09513 · Cited by 2,128
Monocytes and macrophages: developmental pathways and tissue homeostasis
Ginhoux, F., & Jung, S. (2014) · Nature Reviews Immunology · doi:10.1038/nri3671 · Cited by 1,840
Self-citationSerbina, N. V., & Pamer, E. G. (2006) · Nature Immunology · doi:10.1038/ni1309 · Cited by 1,658
Epelman, S., Lavine, K. J., Beaudin, A. E., Sojka, D. K., Carrero, J. A., Calderon, B., Brija, T., Gautier, E. L., Ivanov, S., Satpathy, A. T., et al. (2014) · Immunity · doi:10.1016/j.immuni.2013.11.019 · Cited by 1,494
Self-citationMicroglia emerge from erythromyeloid precursors via Pu.1- and Irf8-dependent pathways
Kierdorf, K., Erny, D., Goldmann, T., Sander, V., Schulz, C., Perdiguero, E. G., Wieghofer, P., Heinrich, A., Riemke, P., Hölscher, C., et al. (2013) · Nature Neuroscience · doi:10.1038/nn.3318 · Cited by 1,457
Jenkins, S. J., Rückerl, D., Cook, P. C., Jackson-Jones, L. H., Finkelman, F. D., van Rooijen, N., MacDonald, A. S., & Allen, J. E. (2011) · Science · doi:10.1126/science.1204351 · Cited by 1,404
TGF-ß Signaling in Fibroblasts Modulates the Oncogenic Potential of Adjacent Epithelia
Bhowmick, N. A., Chytil, A., Plieth, D., Gorska, A. E., Dumont, N., Shappell, S., Washington, M. K., Neilson, E. G., & Moses, H. L. (2004) · Science · doi:10.1126/science.1090922 · Cited by 1,401
Guilliams, M., de Kleer, I., Henri, S., Post, S., Vanhoutte, L., Prijck, S. D., Deswarte, K., MALISSEN, B., Hammad, H., & Lambrecht, B. N. (2013) · The Journal of Experimental Medicine · doi:10.1084/jem.20131199 · Cited by 1,342
Bain, C. C., Bravo-Blas, A., Scott, C. L., Gomez Perdiguero, E., Geissmann, F., Henri, S., Malissen, B., Osborne, L. C., Artis, D., & Mowat, A. M. (2014) · Nature Immunology · doi:10.1038/ni.2967 · Cited by 1,178
van Furth, R., Cohn, Z. A., Jg, H., Humphrey, J., Spector, W. G., & Langevoort, H. L. (1972) · PubMed Central · Cited by 1,133
Development of erythroid and myeloid progenitors in the yolk sac and embryo proper of the mouse
Palis, J., Robertson, S. M., Kennedy, M., Wall, C., & Keller, G. M. (1999) · Development · doi:10.1242/dev.126.22.5073 · Cited by 1,095
A functional c-myb gene is required for normal murine fetal hepatic hematopoiesis
Mucenski, M. L., McLain, K., Kier, A. B., Swerdlow, S. H., Schreiner, C. M., Miller, T. A., Pietryga, D. W., Scott, W. J., & Potter, S. S. (1991) · Cell · doi:10.1016/0092-8674(91)90099-k · Cited by 1,028
Moore, M. A. S., & Metcalf, D. (1970) · British Journal of Haematology · doi:10.1111/j.1365-2141.1970.tb01443.x · Cited by 1,015
Hoeffel, G., Wang, Y., Greter, M., See, P., Teo, P., Malleret, B., Leboeuf, M., Low, D., Oller, G., Almeida, F., et al. (2012) · Journal of Experimental Medicine · doi:10.1084/jem.20120340 · Cited by 786
Self-citationTamoutounour, S., Guilliams, M., Montanana Sanchis, F., Liu, H., Terhorst, D., Malosse, C., Pollet, E., Ardouin, L., Luche, H., Sanchez, C., et al. (2013) · Immunity · doi:10.1016/j.immuni.2013.10.004 · Cited by 783
Jakubzick, C. V., Gautier, E., Gibbings, S. L., Sojka, D. K., Schlitzer, A., Johnson, T. E., Ivanov, S., Duan, Q., Bala, S., Condon, T., et al. (2013) · Immunity · doi:10.1016/j.immuni.2013.08.007 · Cited by 762
Self-citationOf lineage and legacy: the development of mammalian hematopoietic stem cells
Dzierzak, E., & Speck, N. A. (2008) · Nature Immunology · doi:10.1038/ni1560 · Cited by 707
Origin of monocytes and macrophages in a committed progenitor
Hettinger, J., Richards, D. M., Hansson, J., Barra, M. M., Joschko, A.-C., Krijgsveld, J., & Feuerer, M. (2013) · Nature Immunology · doi:10.1038/ni.2638 · Cited by 706
Microglia Modulate Wiring of the Embryonic Forebrain
Squarzoni, P., Oller, G., Hoeffel, G., Pont‐Lezica, L., Rostaing, P., Low, D., Bessis, A., Ginhoux, F., & Garel, S. (2014) · Cell Reports · doi:10.1016/j.celrep.2014.07.042 · Cited by 697
Self-citationMYB function in normal and cancer cells
Ramsay, R. G., & Gonda, T. J. (2008) · Nature reviews. Cancer · doi:10.1038/nrc2439 · Cited by 630
Schneider, C., Nobs, S. P., Kurrer, M. O., Rehrauer, H., Thiele, C., & Köpf, M. (2014) · Nature Immunology · doi:10.1038/ni.3005 · Cited by 629
Cell tracing shows the contribution of the yolk sac to adult haematopoiesis
Samokhvalov, I. M., Samokhvalova, N. I., & Nishikawa, S. (2007) · Nature · doi:10.1038/nature05725 · Cited by 481
Self-citationPalis, J., & Yöder, M. C. (2001) · Experimental Hematology · doi:10.1016/s0301-472x(01)00669-5 · Cited by 468
Primitive and definitive erythropoiesis in mammals
Palis, J. (2014) · Frontiers in Physiology · doi:10.3389/fphys.2014.00003 · Cited by 442
Kumaravelu, P., Hook, L., Morrison, A. M., Ure, J. M., Zhao, S., Zuyev, S., Ansell, J., & Medvinsky, A. (2002) · Development · doi:10.1242/dev.129.21.4891 · Cited by 435
Embryonic origin of the adult hematopoietic system: advances and questions
Medvinsky, A., Александрович, Р. С., & Taoudi, S. (2011) · Development · doi:10.1242/dev.040998 · Cited by 426
Characterization of Definitive Lymphohematopoietic Stem Cells in the Day 9 Murine Yolk Sac
Yöder, M. C., Hiatt, K. K., Dutt, P., Mukherjee, P., Bodine, D. M., & Orlic, D. (1997) · Immunity · doi:10.1016/s1074-7613(00)80355-6 · Cited by 419
Circulation and Chemotaxis of Fetal Hematopoietic Stem Cells
Christensen, J. L., Wright, D. E., Wagers, A. J., & Weissman, I. L. (2004) · PLoS Biology · doi:10.1371/journal.pbio.0020075 · Cited by 376
Transcriptional regulation of granulocyte and monocyte development
Friedman, A. D. (2002) · Oncogene · doi:10.1038/sj.onc.1205324 · Cited by 333
Three pathways to mature macrophages in the early mouse yolk sac
Bertrand, J. Y., Jalil, A., Klaine, M., Jung, S., Cumano, A., & Godin, I. (2005) · Blood · doi:10.1182/blood-2005-02-0461 · Cited by 315
Embryonic development of the human hematopoietic system
Tavian, M., & Peault, B. (2005) · The International Journal of Developmental Biology · doi:10.1387/ijdb.041957mt · Cited by 311
Böiers, C., Carrelha, J., Lutteropp, M., Luc, S., Green, J. C. A., Azzoni, E., Woll, P. S., Mead, A. J., Hultquist, A., Swiers, G., et al. (2013) · Cell stem cell · doi:10.1016/j.stem.2013.08.012 · Cited by 279
Boyer, S. W., Schroeder, A. V., Smith‐Berdan, S., & Forsberg, E. C. (2011) · Cell stem cell · doi:10.1016/j.stem.2011.04.021 · Cited by 245
Self-citationTakahashi, K., Yamamura, F., & Naito, M. (1989) · Journal of Leukocyte Biology · doi:10.1002/jlb.45.2.87 · Cited by 242
Functional hierarchy of c-kit and c-fms in intramarrow production of CFU-M.
Sudo, T., Nishikawa, S., Ogawa, M., Kataoka, H., Ohno, N., Izawa, A., Hayashi, S., & Nishikawa, S. (1995) · PubMed · Cited by 167
Frame, J. M., McGrath, K. E., & Palis, J. (2013) · Blood Cells Molecules and Diseases · doi:10.1016/j.bcmd.2013.09.006 · Cited by 167
Embryonic Origin of the Mouse Macrophage
Cline, M. J., & Moore, M. A. S. (1972) · Blood · doi:10.1182/blood.v39.6.842.842 · Cited by 126
Immature hematopoietic stem cells undergo maturation in the fetal liver
Kieusseian, A., de la Grange, P. B., Burlen‐Defranoux, O., Godin, I., & Cumano, A. (2012) · Development · doi:10.1242/dev.079210 · Cited by 121
Development, Differentiation, and Maturation of Macrophages in the Fetal Mouse Liver
Naito, M., Takahashi, K., & Nishikawa, S.-L. (1990) · Journal of Leukocyte Biology · doi:10.1002/jlb.48.1.27 · Cited by 115
Sumner, R., Crawford, A., Mucenski, M. L., & Frampton, J. (2000) · Oncogene · doi:10.1038/sj.onc.1203660 · Cited by 115
Golub, R., & Cumano, A. (2013) · Blood Cells Molecules and Diseases · doi:10.1016/j.bcmd.2013.08.004 · Cited by 113
Macrophages: Gatekeepers of Tissue Integrity
Lavin, Y., & Mérad, M. (2013) · Cancer Immunology Research · doi:10.1158/2326-6066.cir-13-0117 · Cited by 104
Self-citationLymphoid Progenitor Emergence in the Murine Embryo and Yolk Sac Precedes Stem Cell Detection
Lin, Y., Yöder, M. C., & Yoshimoto, M. (2014) · Stem Cells and Development · doi:10.1089/scd.2013.0536 · Cited by 80
FLT3 expression initiates in fully multipotent mouse hematopoietic progenitor cells
Buza-Vidas, N., Woll, P. S., Hultquist, A., Duarte, S., Lutteropp, M., Bouriez‐Jones, T., Ferry, H., Luc, S., & Jacobsen, S. E. W. (2011) · Blood · doi:10.1182/blood-2010-10-316232 · Cited by 70
Transcriptional Control of Macrophage Identity, Self-Renewal, and Function
Molawi, K., & Sieweke, M. H. (2013) · Advances in immunology · doi:10.1016/b978-0-12-417028-5.00010-7 · Cited by 58
Clarke, D., Vegiopoulos, A., Crawford, A., Mucenski, M. L., Bonifer, C., & Frampton, J. (2000) · Oncogene · doi:10.1038/sj.onc.1203661 · Cited by 42
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Metadata
- Authors
- Hoeffel, G., Chen, J., Lavin, Y., Low, D., Almeida, F. F., See, P., Beaudin, A. E., Lum, J., Low, I., Forsberg, E. C., Poidinger, M., Zolezzi, F., Larbi, A., Ng, L. G., Chan, J. K. Y., Greter, M., Becher, B., Samokhvalov, I. M., Merad, M., & Ginhoux, F.
- Affiliations
- Agency for Science, Technology and Research (SG)
- Tisch Cancer Institute (US)
- University of California, Santa Cruz (US)
- University of Zurich (CH)
- Chinese Academy of Sciences (CN)
- Corresponding author
- Ginhoux, Florent
- ORCID
- Venue
- Immunity
- Publisher
- Elsevier BV
- Published
- 2015-04
- Volume
- 42
- Issue
- 4
- Pages
- 665-678
- ISSN
- 1074-7613 (ISSN-L)
- PMC
- PMC4545768
- OpenAlex
- W2023666964
- Cited by
- 1,135
- References
- 55
- Citations by year
- 2026: 64 · 2025: 84 · 2024: 111 · 2023: 99 · 2022: 135 · 2021: 122 · 2020: 118 · 2019: 102 · 2018: 107 · 2017: 81 · 2016: 67 · 2015: 44
- FWCI
- 77.82
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- Immunity (publishedVersion)
- PubMed (publishedVersion)
- PubMed Central (acceptedVersion)
- Zurich Open Repository and Archive (University of Zurich) (acceptedVersion)
- National University of Singapore (submittedVersion)
- Zurich Open Repository and Archive (University of Zurich) (submittedVersion)
- Funders
- National Heart, Lung, and Blood Institute (HL086899, R01HL086899)
- National Cancer Institute (R01CA173861, R01CA112100, CA112100, R01CA190400)
- National Institute of Allergy and Infectious Diseases (AI080884, R01AI080884)
- National Institute of Diabetes and Digestive and Kidney Diseases (R01DK100917)
- Topics
- Health Sciences › Medicine › Hematology › Hematopoietic Stem Cell Transplantation
- Life Sciences › Immunology and Microbiology › Immunology › Immune cells in cancer
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Developmental Biology and Gene Regulation
- Keywords
- tissue-resident macrophages, erythro-myeloid progenitors, microglia, yolk sac hematopoiesis, fetal liver hematopoiesis, MYB, fate mapping
- MeSH terms
- Aging, Animals, Cell Differentiation, Embryo, Mammalian, Female, Fetus, Hematopoietic Stem Cells, Kidney, Liver, Lung, Macrophages, Monocytes, Pregnancy, Skin, Yolk Sac, Biomarkers, Microglia, Cell Lineage, Proto-Oncogene Proteins c-myb, Myeloid Progenitor Cells, Mice, Cell Tracking, Primary Cell Culture
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